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MR Cholangiopancreatographic Differentiation of Benign and Malignant Intraductal Mucin- Producing Tumors of the Pancreas

¹ Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku Fukuoka, 812-8582 Japan.
² Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku Fukuoka, 812-8582 Japan.
³ Department of General Surgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku Fukuoka, 812-8582 Japan.

Received September 20, 1999; accepted after revision November 1, 1999.

 
Address correspondence to H. Irie.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. The purpose of this study was to establish MR cholangiopancreatographic criteria for discriminating benign from malignant intraductal mucin-producing tumors of the pancreas.

MATERIALS AND METHODS. Thirty-one patients with 34 intraductal mucin-producing tumors underwent MR cholangiopancreatography. Tumors were classified as either main duct type (n = 10) or branch duct type (n = 24). In patients with the main duct type, the maximum diameter and the location of the main pancreatic duct, the extent of main pancreatic duct dilatation, and the presence of a filling defect were evaluated. For branch duct type, the location and maximum diameter of the cystic lesion, the presence of a filling defect, and the presence of associated main pancreatic duct dilatation were evaluated.

RESULTS. In patients with the main duct type, the main pancreatic duct was significantly narrower when associated with benign rather than malignant tumors. All malignant tumors showed diffuse main pancreatic duct dilatation, whereas all benign tumors showed segmental dilatation. Among patients with branch duct type, the cyst was smaller when it was a benign rather than malignant tumor. All but one malignant tumor showed mild associated main pancreatic duct dilatation, whereas benign tumors were not associated with main pancreatic duct dilatation. Filling defects suggested malignancy, although half of the malignant tumors had no filling defects.

CONCLUSION. In patients with intraductal mucin-producing tumors of the pancreas, filling defects are indicative of malignancy. Diffuse main pancreatic duct dilatation greater than 15 mm (main duct type), or any main pancreatic duct dilatation (branch duct type), is strongly associated with malignancy.

Introduction

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Intraductal mucin-producing tumors of the pancreas were first described by Ohhashi et al. [1] in 1982. These tumors are characterized by massive production and retention of mucin in the pancreatic duct and interstitium, dilatation of the papilla of Vater caused by mucinous flow, little tendency for infiltration, and a good prognosis [2, 3]. The lesion may originate from the main pancreatic duct or its collateral branches and thus may be classified as a main duct type or branch duct type [1, 4]. Pathologically, a wide spectrum of benign and malignant abnormalities has been described, including nonneoplastic hyperplasia, adenoma, borderline (adenoma with severe atypia), and adenocarcinoma [5]. Until the mid 1980s, intraductal mucin-producing tumors of the pancreas were considered rare, and most reported cases occurred in Japan. Recently, however, the number of reported cases has increased dramatically, not only in Japan but also in the Western world [6]. It is likely that some of these tumors have been incorrectly interpreted as sequela of chronic obstructive pancreatitis because of the macroscopic features of the tumor and the clinical history of the patient [7].

Sonography and CT are useful in the diagnosis of intraductal mucin-producing tumors of the pancreas. Main duct-type tumors are characterized by either diffuse or segmental dilatation of the main pancreatic duct. Branch duct-type tumors appear as clusters of small cysts or as a single cystic lesion with lobulated or irregular margins and sparse septa, often with dilatation of the pancreatic duct near the lesion [8,9,10]. Endoscopic retrograde cholangiopancreatography (ERCP), however, is mandatory for the diagnosis of an intraductal mucin-producing tumor of the pancreas [8, 10,11,12]. ERCP can show diffuse and segmental main pancreatic duct dilatation without stricture as well as localized cystic dilatation of a branch duct and filling defects. However, ERCP has some drawbacks: acute pancreatitis occurs in 5% of patients after the examination [13], technical failure is possible [14], and some patients cannot tolerate an endoscopic examination.

MR imaging technology has made it possible to visualize the pancreatic and bile ducts without the use of contrast material [15, 16], and many researchers have compared the usefulness of MR cholangiopancreatography (MRCP) and ERCP in the evaluation of biliary and pancreatic disorders [16,17,18]. In several recent reports, investigators compared MRCP and ERCP in evaluating mucin-producing tumors of the pancreas [19,20,21,22,23]. Most of these investigators reported the superiority of MRCP to ERCP in evaluating intraductal mucin-producing tumors of the pancreas and concluded that MRCP is the first and best choice among imaging techniques in assessing these lesions.

Because intraductal mucin-producing tumors of the pancreas encompass a wide range of histologic findings—from apparently benign to overtly malignant—and are reported to be slow-growing [24], some patients with intraductal mucin-producing tumors of the pancreas can be monitored without undergoing surgery [7]. In addition, the surgical strategy may be altered by the grade of malignancy of the tumor [25]. Therefore, radiologic differentiation between benign and malignant lesions is important in determining the appropriate treatment. Previous methods for determining the likelihood of malignancy [5, 7, 24, 25] have been based mainly on clinical and ERCP findings. To our knowledge, the utility of performing MRCP to differentiate benign and malignant intraductal mucin-producing tumors of the pancreas has not been reported.

We reviewed MRCP findings of surgically resected intraductal mucin-producing tumors of the pancreas to establish MRCP criteria for predicting malignancy.

Materials and Methods

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Between May 1995 and February 1999, 31 patients at our institution were diagnosed with intraductal mucin-producing tumors by histologic examination of surgical specimens. Three patients had two tumors, hence 34 tumors were included in the study. All patients underwent MRCP within 1 month before surgery. Twenty-one men and 10 women, who ranged in age from 46 to 79 years (mean, 68 years), comprised our study group. Tumors were classified as main duct type or branch duct type, according to the location (main pancreatic duct or branch duct) of the tumor and the criteria of Nakazawa et al. [3]. There were 10 main duct-type tumors in 10 patients (eight men and two women) and 24 branch duct-type tumors in 21 patients (12 men and nine women). Histologically, tumors were diagnosed as adenoma, adenocarcinoma, or borderline lesion. A borderline lesion was defined as a tumor that was not overtly malignant but had some foci of severe cellular atypia, indicating that it should be treated as a malignant tumor. There were four adenomas, three borderline lesions, and three adenocarcinomas among the main duct-type tumors, and 17 adenomas, five borderline lesions, and two adenocarcinomas among the branch duct-type tumors. Main duct-type tumors were sited in the head of the pancreas in five patients (adenoma, n = 2; borderline lesion, n = 1; adenocarcinoma, n = 2), in the body in four (adenoma, n = 1; borderline lesion, n = 2; adenocarcinoma, n = 1), and in the tail in one (adenoma). Branch duct-type tumors were sited in the pancreatic head in 16 patients (adenoma, n = 11; borderline lesion, n = 5), in the body in seven (adenoma, n = 5; adenocarcinoma, n = 2), and in the tail in one (adenoma).

MRCP acquisition was performed on a 1.5-T superconducting MR unit (Magnetom Vision; Siemens, Erlangen, Germany) using a half-Fourier single-shot turbo spin-echo sequence with a phased array coil. A 240 x 256 matrix and a 250 x 250 mm field of view were used with fat suppression. Because HASTE is a single-shot sequence, there is no TR. The effective TE and echo train length were 87 and 128 msec, respectively. Two different data acquisition techniques were applied: sequential multislice imaging with a 5-mm slice thickness followed by maximum-intensity-projection reconstruction and single-slice projection imaging using a thick-slice technique (3-7 cm, depending on pancreatic thickness). The imaging time was less than 2 sec per slice, and the total time for sequential multislice imaging was 14-26 sec, depending on pancreatic thickness. Coronal planes, oblique coronal planes, or both planes were used in both techniques, according to the site of the lesion. Images were acquired during a single breath-hold.

MRCP findings were reviewed retrospectively. Both maximum-intensity-projection reconstruction with its source images and single-slice projection images were provided for evaluation. For main duct-type tumors, we analyzed the maximum diameter and location of the main pancreatic duct, the extent of main pancreatic duct dilatation, and the presence of a filling defect within the main pancreatic duct. For branch duct-type tumors, the location and maximum diameter of the cystic lesion, the presence of a filling defect within the lesion, and the presence of associated main pancreatic duct dilatation were evaluated. The maximum diameters of the main pancreatic duct and the cystic lesions were measured on the MR console. The main pancreatic duct was defined as dilated when its diameter was greater than 5 mm. These factors were separately interpreted by two radiologists who did not know the pathologic findings. In cases of interobserver disagreement, final decisions were reached by consensus. For filling defects within the main pancreatic duct or the cystic lesion, MRCP findings were compared with the macroscopic pathologic findings. Statistical analysis comparing benign tumors (adenomas) to malignant tumors (borderline lesions and adenocarcinomas) was performed using one-way factorial analysis of variance.

Results

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Main Duct-Type Tumors
The maximum diameter of the main pancreatic duct in cases of benign tumors (n = 4) ranged from 10 to 12 mm, with a mean of 11 mm (Fig. 1). Malignant tumors (n = 6) ranged from 15 to 30 mm in diameter, with a mean of 20 mm (Fig. 2). This difference was statistically significant (p < 0.05). The location of maximum main pancreatic duct dilatation in benign tumors was in the head in two tumors, the body in one tumor, and the tail in one tumor. Among malignant tumors, the maximum main pancreatic duct dilatation was located in the head in three and in the body in three. There was no significant difference in the location of maximum main pancreatic duct dilatation between benign and malignant tumors. The location of maximum main pancreatic duct dilatation was identical to the site of the main neoplastic lesion in all patients. Among benign tumors, main pancreatic duct dilatation was limited to one or two pancreatic segments of the main pancreatic duct (Fig. 1). The main pancreatic duct was dilated diffusely in all malignant tumors (Fig. 2). MRCP did not show a filling defect within the main pancreatic duct in benign tumors, although macroscopic examination of the specimen revealed a small mural nodule 3 mm in diameter in one patient (one false-negative case). Among malignant tumors, filling defects larger than 10 mm in diameter were detected in three patients, all of which were confirmed by examination of the pathologic specimen (Fig. 3A,3B). In one malignant tumor, MRCP showed a small filling defect of less than 5 mm in diameter; however, macroscopic examination of the specimen revealed no mural nodule within the main pancreatic duct (one false-positive case). There was no false-negative case among the malignant tumors. MRCP findings of the main duct-type tumors are summarized in Table 1.

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —78-year-old man with benign (adenoma) main duct-type intraductal mucin-producing tumor of pancreas. Maximum-intensity-projection MR cholangiopancreatogram shows main pancreatic duct (long straight arrows) dilated in body and tail, but not in head. Maximum diameter of main pancreatic duct is 12 mm. Nondilated main pancreatic duct (short straight arrows), measuring 4 mm in diameter, and common bile duct (curved arrows) can be seen.

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —60-year-old man with malignant (borderline) main duct-type intraductal mucin-producing tumor of pancreas. Maximum-intensity-projection MR cholangiopancreatogram reveals main pancreatic duct with markedly diffuse dilatation. Maximum diameter of main pancreatic duct is 25 mm. PD = pancreatic duct.

View larger version (76K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —71-year-old man with malignant (adenocarcinoma) main duct-type intraductal mucin-producing tumor of pancreas. PD = pancreatic duct. Maximum-intensity-projection MR cholangiopancreatogram shows diffuse dilatation of main pancreatic duct (maximum diameter, 20 mm).

View larger version (86K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —71-year-old man with malignant (adenocarcinoma) main duct-type intraductal mucin-producing tumor of pancreas. PD = pancreatic duct. Source MR cholangiopancreatographic image reveals filling defects (arrows) in main pancreatic duct of pancreatic body.

Branch Duct-Type Tumors
The maximum diameter of benign branch duct-type tumors (n = 17) ranged from 10 to 45 mm, with a mean of 24 mm (Fig. 4). The maximum diameter of malignant tumors (n = 7) ranged from 20 to 55 mm, with a mean of 35 mm (Fig. 5). This difference was statistically significant (p < 0.05), although there were some overlaps (Figs. 6 and 7). Eleven benign tumors were located in the pancreatic head, five in the body, and one in the tail. Five malignant tumors were located in the head and two were in the body. There was no significant difference in the location of the cystic lesion between benign and malignant tumors. No filling defect was seen on MRCP in the benign tumors. This was confirmed by examination of the pathologic specimens. In contrast, a filling defect was detected on MRCP in three of seven malignant tumors (Fig. 8), which corresponded to mural nodules in the pathologic specimens. There was no main pancreatic duct dilatation associated with benign tumors (Fig. 4). All but one malignant tumor showed mild associated main pancreatic duct dilatation (Figs. 5, 7, and 8), ranging from 5 to 10 mm. MRCP findings of the branch duct-type tumors are summarized in Table 2.

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4. —65-year-old man with benign (adenoma) branch duct-type intraductal mucin-producing tumor of pancreas. Single-slice projection MR cholangiopancreatographic image reveals multilocular cystic lesion (arrows) in pancreatic head and communicates with nondilated main pancreatic duct. Maximum diameter of cyst is 20 mm.

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —65-year-old man with malignant (borderline) branch duct-type intraductal mucin-producing tumor of pancreas. Maximum-intensity-projection MR cholangiopancreatogram shows grapelike cluster of cysts (straight arrows) with maximum diameter of 55 mm in pancreatic head. Main pancreatic duct in head and body shows mild dilatation. Another small cystic lesion (curved arrow), which was not resected at surgery, is seen in pancreatic tail.

View larger version (6K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —Scatterplot of cyst size of benign (n = 17) and malignant (n = 7) branch duct-type mucin-producing tumor of pancreas. Graph shows some overlap between them.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7. —67-year-old man with malignant (borderline) branch duct-type intraductal mucin-producing tumor of pancreas. Maximum-intensity-projection MR cholangiopancreatogram shows multilocular cystic lesion (arrows) in pancreatic head. Maximum size of cyst is 25 mm; however, main pancreatic duct shows mild diffuse dilatation.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8. —69-year-old man with malignant (adenocarcinoma) branch duct-type intraductal mucin-producing tumor of pancreas. Single-projection MR cholangiopancreatographic image shows cyst with large filling defect (arrows) in pancreatic body. Main pancreatic duct shows mild dilatation in body and tail.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The MRCP characteristics of intraductal mucin-producing tumors of the pancreas have recently been described [19,20,21,22,23]. In main duct-type tumors, MRCP shows moderate to marked, and usually diffuse, dilatation of the main pancreatic duct. Branch duct-type tumors show grapelike clusters of cysts with mild or absent dilatation of the main pancreatic duct [19]. Sometimes mural nodules are seen as filling defects within the main pancreatic duct or the cystic lesion [19]. These imaging findings are relatively specific to intraductal mucin-producing tumors of the pancreas, and diagnosis can usually be established using MRCP, although it is often difficult to differentiate a main duct-type mucin-producing tumor from chronic pancreatitis and a branch duct-type mucin-producing tumor from a pancreatic pseudocyst with ductal communication. Comparisons between the MRCP findings and ERCP findings in patients with intraductal mucin-producing tumors of the pancreas have been reported [19,20,21,22,23]. Although Usuki et al. [23] reported that MRCP and ERCP are complementary techniques for imaging intraductal mucin-producing tumors of the pancreas, other researchers have concluded that MRCP is more sensitive and effective than ERCP in evaluating these tumors [19,20,21,22]. The reason MRCP is better than ERCP at depicting the dilated main pancreatic duct and cystic lesions is that mucinous fluid produced by the tumor or the tumor itself inhibits adequate inflow of the contrast material into the main pancreatic duct or the cystic dilated branches [20]. In addition, intraductal mucin, as a result of its high signal intensity, is indistinguishable from pancreatic juice on MRCP, whereas mural nodules are seen as filling defects. MRCP is thus more sensitive than ERCP in diagnosing mural nodules [19]. However, Koito et al. [20] have stated that MRCP does not offer any pathologic information to decide whether the lesions are malignant.

Correct prediction of malignancy remains one of the most difficult problems in the management of intraductal mucin-producing tumors of the pancreas [26]. The grade of malignancy is important in determining the appropriate surgical procedure [25], and benign tumors may be followed up without surgery [5]. In several reports, investigators have used imaging findings to determine the likelihood of malignancy [27,28,29]. These authors evaluated the size and type of the lesions, the diameter of the main pancreatic duct, and the presence of mural nodules. Kobayashi et al. [27] reported that irregularities of the ductal wall, a thickened septum, and masses protruding into the dilated duct were present in adenocarcinoma and adenoma, but not in hyperplasia. Yanagisawa et al. [28] noted that adenocarcinomas tended to be larger than adenomas (50 and 30 mm in diameter, respectively). Obara et al. [29] reported that 83% of the tumors larger than 4 cm in diameter, either of the main duct or branch duct type, were malignant, whereas the branch duct-type tumors of less than 3 cm without marked dilatation of the main pancreatic duct or excrescent nodules were invariably benign; these reports were based on findings obtained using ERCP or sonography. Recently, Sugiyama and Atomi [26] reviewed sonographic, CT, endoscopic sonographic, ERCP, and MRCP findings of intraductal mucin-producing tumors of the pancreas and reported that a main pancreatic duct diameter of greater than 15 mm or a tumor diameter of greater than 30 mm in branch duct-type tumors indicated a high likelihood of malignancy. In addition, 64% of tumors with mural nodules showed invasion. However, the number of MRCP examinations performed was fairly small (11/41 tumors studied), and the imaging protocol used to determine the characteristics of each tumor was not reported.

We analyzed the MRCP findings of intraductal mucin-producing tumors of the pancreas to identify signs indicative of malignancy. As has been described in reports on ERCP or other imaging techniques [5, 25,26,27], mural nodules were highly suggestive of malignancy. Four of six malignant main duct-type tumors and three of seven malignant branch duct-type tumors showed filling defects within the dilated main pancreatic duct or the cystic lesion (although the filling defect in one main duct-type tumor was considered a false-negative finding). Among the benign tumors of either main duct or branch duct type, mural nodules were not seen, although there was one false-negative finding in a main duct-type tumor that was smaller than 5 mm. Diagnostic accuracy in detecting mural nodules using MRCP was 80% for main duct-type tumors and 100% for branch duct-type tumors. Approximately half of malignant tumors did not have mural nodules within the lesion. Sugiyama and Atomi [26] reported that 37% of tumors without mural nodules were malignant. Histologic diagnosis mainly depends on the nuclear-cytoplasmic ratio, nuclear hyperchromasia, and the shape of the nuclei. Therefore, a papillary projection itself does not indicate malignancy [30]. Detection of mural nodules within intraductal mucin-producing tumors of the pancreas is associated with malignancy. However, absence of mural nodules does not indicate that the tumor is benign, and other MRCP findings should be evaluated.

In main duct-type tumors, the location of maximum main pancreatic duct dilatation was identical for benign and malignant tumors. However, this location correlated with the site of the tumor and may be helpful in planning surgical resection when no mural nodules are detected and the tumor site cannot be determined. The maximum diameter of the main pancreatic duct differed significantly between benign and malignant tumors. A maximum main pancreatic duct diameter of 15 mm may indicate malignancy. Another important factor is the extent of main pancreatic duct dilatation, because the main pancreatic duct was dilated diffusely in all malignant tumors but was dilated segmentally in all benign tumors. The maximum diameter of the main pancreatic duct and the extent of the dilatation are considered to be a consequence of the amount of mucin that the tumor produces. Malignant intraductal mucin-producing tumors of the pancreas may produce more mucin than benign tumors.

In branch duct-type tumors, the size of the cystic lesion differed significantly between benign and malignant tumors. A cyst diameter of 30 mm or greater may suggest malignancy, as previously suggested in reports using ERCP and other imaging techniques [25, 26, 29]. The cyst size alone, however, should not be used as a sole indicator of malignancy because considerable overlap between the cyst size of benign and malignant tumors was found. Main pancreatic dilatation may be a more reliable differentiating factor: no significant main pancreatic duct dilatation was seen in any benign tumor, whereas six of seven malignant tumors showed mild main pancreatic duct dilatation. Main duct-type tumors tend to have a higher grade of malignancy compared with that of branch duct-type tumors [5,6,7]. In our study, 60% of main duct-type tumors and 26% of branch duct-type tumors were malignant. Four of six branch duct-type tumors with associated main pancreatic duct dilatation revealed some foci of neoplastic changes in the main pancreatic duct. These foci may represent the more malignant nature of these branch duct-type tumors that involve the main pancreatic duct. We believe that the most important factor in differentiating between benign and malignant branch duct-type tumors is the presence of main pancreatic duct dilatation.

In conclusion, MRCP is useful in differentiating benign and malignant intraductal mucin-producing tumors of the pancreas. The presence of mural nodules is suggestive of malignancy. However, the absence of mural nodules does not indicate that the tumor is benign. A maximum main pancreatic duct diameter of greater than 15 mm and diffuse dilatation of the main pancreatic duct are suggestive of malignancy in main duct-type tumors. Among branch duct-type tumors, malignant tumors tend to be larger than benign tumors; however, this finding is variable. The presence of main pancreatic duct dilatation may be helpful in determining malignancy of branch duct-type tumors.

References

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